Hypoxia. 1. Intracellular sensors for oxygen and oxidative stress: Novel therapeutic targets

American Journal of Physiology - Cell Physiology

Volumn 300, Issue 2, 2011, Pages

  Miyata, Toshio ^a   Takizawa, Shunya ^a   Van Ypersele De Strihou, Charles ^a  

^a NONE

Author keywords

Hypoxia; Hypoxia inducible factor; Kelch like ECH associated protein 1; Nuclear factor erythroid 2 p45 related factor 2; Oxygen sensor; Prolylhydroxylase

Indexed keywords

ANTIOXIDANT; BARDOXOLONE METHYL; DIMETHYLOXALYLGLYCINE; ENZYME INHIBITOR; HYPOXIA INDUCIBLE FACTOR; ISOENZYME; KELCH LIKE ECH ASSOCIATED PROTEIN 1; LEVO MINOSINE; N OXALYLGLYCINE; N OXALYLPHENYLALANINE; OXALIC ACID DERIVATIVE; OXYGEN; PHENYLALANINE DERIVATIVE; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROTEIN INHIBITOR; TM 6008; TM 6089; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

BIOSENSOR; CLINICAL TRIAL; DIABETIC NEPHROPATHY; ENZYME INHIBITION; HUMAN; HYPOXIA; MITOCHONDRION; NONHUMAN; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; TISSUE INJURY;

ANGIOGENESIS INDUCING AGENTS; ANIMALS; ANOXIA; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MITOCHONDRIA; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; OXYGEN; PROCOLLAGEN-PROLINE DIOXYGENASE; PROTEASE INHIBITORS; RATS;

ANIMALIA;

EID: 79251535600     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00430.2010     Document Type: Review

References (69)

1. Aragonés J, Schneider M, Van Geyte K, Fraisl P, Dresselaers T, Mazzone M, Dirkx R, Zacchigna S, Lemieux H, Jeoung NH, Lambrechts D, Bishop T, Lafuste P, Diez-Juan A, Harten SK, Van Noten P, De Bock K, Willam C, Tjwa M, Grosfeld A, Navet R, Moons L, Vandendriessche T, Deroose C, Wijeyekoon B, Nuyts J, Jordan B, Silasi-Mansat R, Lupu F, Dewerchin M, Pugh C, Salmon P, Mortelmans L, Gallez B, Gorus F, Buyse J, Sluse F, Harris RA, Gnaiger E, Hespel P, Van Hecke P, Schuit F, Van Veldhoven P, Ratcliffe P, Baes M, Maxwell P, Carmeliet P. Deficiency or inhibition of oxygen sensor Phd1 induces hypoxia tolerance by reprogramming basal metabolism. Nat Genet 40: 170-180, 2008. (Pubitemid 351171394)
2. Berchner-Pfannschmidt U, Tug S, Trinidad B, Oehme F, Yamac H, Wotzlaw C, Flamme I, Fandrey J. Nuclear oxygen sensing: induction of endogenous prolyl-hydroxylase 2 activity by hypoxia and nitric oxide. J Biol Chem 283: 31745-31753, 2008.
3. Bergeron M, Yu AY, Solway KE, Semenza GL, Sharp FR. Induction of hypoxia-inducible factor-1 (HIF-1) and its target genes following focal ischaemia in rat brain. Eur J Neurosci 11: 4159-4170, 1999. (Pubitemid 30009246)
4. Berk L, Burchebal JH, Castle WB. Erythropoietic effect of cobalt in patients with or without anemia. N Engl J Med 240: 754-761, 1949.
5. Bernhardt WM, Wiesener MS, Weidemann A, Schmitt R, Weichert W, Lechler P, Campean V, Ong AC, Willam C, Gretz N, Eckardt KU. Involvement of hypoxia-inducible transcription factors in polycystic kidney disease. Am J Pathol 170: 830-842, 2007. (Pubitemid 47339353)
6. Bonnet S, Archer SL, Allalunis-Turner J, Haromy A, Beaulieu C, Thompson R, Lee CT, Lopaschuk GD, Puttagunta L, Bonnet S, Harry G, Hashimoto K, Porter CJ, Andrade MA, Thebaud B, Michelakis ED. A mitochondria-K+ channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth. Cancer Cell 11: 37-51, 2007.
7. Bosch-Marcé M, Okuyama H, Wesley JB, Sarkar K, Kimura H, Liu YV, Zhang H, Strazza M, Rey S, Savino L, Zhou YF, McDonald KR, Na Y, Vandiver S, Rabi A, Shaked Y, Kerbel R, Lavallee T, Semenza GL. Effects of aging and hypoxia-inducible factor-1 activity on angiogenic cell mobilization and recovery of perfusion after limb ischemia. Circ Res 101: 1310-1318, 2007.
8. Chandel NS, McClintock DS, Feliciano CE, Wood TM, Melendez JA, Rodriguez AM, Schumacker PT. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J Biol Chem 275: 25130-25138, 2000.
9. Cho HY, Jedlicka AE, Reddy SP, Kensler TW, Yamamoto M, Zhang LY, Kleeberger SR. Role of NRF2 in protection against hyperoxic lung injury in mice. Am J Respir Cell Mol Biol 26: 175-182, 2002.
10. Cho HY, Reddy SP, Yamamoto M, Kleeberger SR. The transcription factor NRF2 protects against pulmonary fibrosis. FASEB J 18: 1258-1260, 2004. (Pubitemid 39561569)
11. Edwards MS, Curtis JR. Use of cobaltous chloride in anaemia of maintenance hemodialysis patients. Lancet 2: 582-583, 1971.
12. Eguchi H, Ikuta T, Tachibana T, Yoneda Y, Kawajiri K. A nuclear localization signal of human aryl hydrocarbon receptor nuclear translocator/ hypoxia-inducible factor 1beta is a novel bipartite type recognized by the two components of nuclear pore-targeting complex. J Biol Chem 272: 17640-17647, 1997.
13. Epstein AC, Gleadle JM, McNeill LA, Hewitson KS, O'Rourke J, Mole DR, Mukherji M, Metzen E, Wilson MI, Dhanda A, Tian YM, Masson N, Hamilton DL, Jaakkola P, Barstead R, Hodgkin J, Maxwell PH, Pugh CW, Schofield CJ, Ratcliffe PJ. Elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107: 43-54, 2001.
14. Fong GH, Takeda K. Role and regulation of prolyl hydroxylase domain proteins. Cell Death Diff 15: 635-641, 2008.
15. Fraisl P, Aragonés J, Carmeliet P. Inhibition of oxygen sensors as a therapeutic strategy for ischaemic and inflammatory disease. Nat Rev Drug Discov 8: 139-152, 2009.
16. Hill P, Shukla D, Tran MG, Aragones J, Cook HT, Carmeliet P, Maxwell PH. Inhibition of hypoxia inducible factor hydroxylases protects against renal ischemia-reperfusion injury. J Am Soc Nephrol 19: 39-46, 2008.
17. Hon WC, Wilson MI, Harlos K, Claridge TD, Schofield CJ, Pugh CW, Maxwell PH, Ratcliffe PJ, Stuart DI, Jones EY. Structural basis for the recognition of hydroxyproline in HIF-1 alpha by pVHL. Nature 417: 975-978, 2002.
18. Itoh K, Wakabayashi N, Katoh Y, Ishii T, Igarashi K, Engel JD, Yamamoto M. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev 13: 76-86, 1999.
19. Ivan M, Haberberger T, Gervasi DC, Michelson KS, Günzler V, Kondo K, Yang H, Sorokina I, Conaway RC, Conaway JW, Kaelin WG Jr. Biochemical purification and pharmacological inhibition of a mammalian prolyl hydroxylase acting on hypoxia-inducible factor. Proc Natl Acad Sci USA 99: 13459-13464, 2002.
20. Ivan M, Kondo K, Yang H, Kim W, Valiando J, Ohh M, Salic A, Asara JM, Lane WS, Kaelin WG Jr. HIFa targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292: 464-468, 2001.
21. Izuhara Y, Nangaku M, Inagi R, Tominaga N, Aizawa T, Kurokawa K, van Ypersele de Strihou C, Miyata T. Renoprotective properties of angiotensin receptor blockers beyond blood pressure lowering. J Am Soc Nephrol 16: 3631-3641, 2005. (Pubitemid 46211284)
22. Kaelin WG Jr, Ratcliffe PJ. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell 30: 393-402, 2008.
23. Katavetin P, Miyata T, Inagi R, Tanaka T, Sassa R, Ingelfinger JR, Fujita T, Nangaku M. High glucose blunts vascular endothelial growth factor response to hypoxia via the oxidativestress-regulated hypoxia-inducible factor/hypoxia-responsible element pathway. J Am Soc Nephrol 17: 1405-1413, 2006.
24. Kim JW, Tchernyshyov I, Semenza GL, Dang CV. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 3: 177-185, 2006.
25. Kobayashi M, Yamamoto M. Molecular mechanisms activating the Nrf2 Keap1 pathway of antioxidant gene regulation. Antioxid Redox Signal 7: 385-394, 2005.
26. Kojima I, Tanaka T, Inagi R, Kato H, Yamashita T, Sakiyama A, Ohneda O, Takeda N, Sata M, Miyata T, Fujita T, Nangaku M. Protective role of hypoxia-inducible factor-2alpha against ischemic damage and oxidative stress in the kidney. J Am Soc Nephrol 18: 1218-1226, 2007.
27. Kulkarni AC, Kuppusamy P, Parinandi N. Oxygen, the lead actor in the pathophysiologic drama: enactment of the trinity of normoxia, hypoxia, and hyperoxia in disease and therapy. Antioxid Redox Signal 9: 1717-1730, 2007.
28. Ladroue C, Carcenac R, Leporrier M, Gad S, Le Hello C, Galateau- Salle F, Feunteun J, Pouysségur J, Richard S, Gardie B. PHD2 mutation and congenital erythrocytosis with paraganglioma. N Engl J Med 359: 2685-2692, 2008.
29. Lee SH, Wolf PL, Escudero R, Deutsch R, Jamieson SW, Thistlethwaite PA. Early expression of angiogenesis factors in acute myocardial ischemia and infarction. N Engl J Med 342: 626-633, 2000.
30. Leonard MO, Kieran NE, Howell K, Burne MJ, Varadarajan R, Dhakshinamoorthy S, Porter AG, O'Farrelly C, Rabb H, Taylor CT. Reoxygenation-specific activation of the antioxidant transcription factor Nrf2 mediates cytoprotective gene expression in ischemia-reperfusion injury. FASEB J 20: 2624-2626, 2006.
31. Liu M, Grigoryev DN, Crow MT, Haas M, Yamamoto M, Reddy SP, Rabb H. Transcription factor Nrf2 is protective during ischemic and nephrotoxic acute kidney injury in mice. Kidney Int 76: 277-285, 2009.
32. Makino Y, Kanopka A, Wilson WJ, Tanaka H, Poellinger L. Inhibitory PAS domain protein (IPAS) is a hypoxia-inducible splicing variant of the hypoxia-inducible factor-3alpha locus. J Biol Chem 277: 32405-32408, 2002.
33. Marx J. How cells endure low oxygen. Science 303: 1454-1456, 2004.
34. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, Wykoff CC, Pugh CW, Maher ER, Ratcliffe PJ. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399: 271-275, 1999.
35. McDonough MA, McNeill LA, Tilliet M, Papamicaël CA, Chen QY, Banerji B, Hewitson KS, Schofield CJ. Selective inhibition of factor inhibiting hypoxia-inducible factor. J Am Chem Soc 127: 7680-7681, 2005.
36. Metzen E, Berchner-Pfannschmidt U, Stengel P, Marxsen JH, Stolze I, Klinger M, Huang WQ, Wotzlaw C, Hellwig-Bürgel T, Jelkmann W, Acker H, Fandrey J. Intracellular localisation of human HIF-1 alpha hydroxylases: implications for oxygen sensing. J Cell Sci 116: 1319-1326, 2003.
37. Minamishima YA, Moslehi J, Bardeesy N, Cullen D, Bronson RT, Kaelin WG Jr. Somatic inactivation of the PHD2 prolyl hydroxylase causes polycythemia and congestive heart failure. Blood 111: 3236-3244, 2008.
38. Miyata T, van Ypersele de Strihou C. Diabetic nephropathy: a disorder of oxygen metabolism? Nat Rev Nephrol 6: 83-95, 2010.
39. Mole DR, Schlemminger I, McNeill LA, Hewitson KS, Pugh CW, Ratcliffe PJ, Schofield CJ. 2-Oxoglutarate analogue inhibitors of HIF prolyl hydroxylase. Bioorg Med Chem Lett 13: 2677-2680, 2003.
40. Nangaku M, Izuhara Y, Takizawa S, Yamashita T, Fujii-Kuriyama Y, Ohneda O, Yamamoto M, van Ypersele de Strihou C, Hirayama N, Miyata T. A novel class of prolyl hydroxylase inhibitors induces angiogenesis and exerts organ protection against ischemia. Arterioscler Thromb Vasc Biol 27: 2548-2554, 2007.
41. Nguyen T, Sherratt PJ, Pickett CB. Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu Rev Pharmacol Toxicol 43: 233-260, 2003.
42. Ohh M, Park CW, Ivan M, Hoffman MA, Kim TY, Huang LE, Pavletich N, Chau V, Kaelin WG. Ubiquitination of hypoxia-inducible factor requires direct binding to the beta-domain of the von Hippel-Lindau protein. Nat Cell Biol 2: 423-427, 2000.
43. Okada K, Shoda J, Taguchi K, Maher JM, Ishizaki K, Inoue Y, Ohtsuki M, Goto N, Sugimoto H, Utsunomiya H, Oda K, Warabi E, Ishii T, Yamamoto M. Nrf2 counteracts cholestatic liver injury via stimulation of hepatic defense systems. Biochem Biophys Res Commun 389: 431-436, 2009.
44. Pan Y, Mansfield KD, Bertozzi CC, Rudenko V, Chan DA, Giaccia AJ, Simon MC. Multiple factors affecting cellular redox status and energy metabolism modulate hypoxia-inducible factor prolyl hydroxylase activity in vivo and in vitro. Mol Cell Biol 7: 912-925, 2007.
45. Percy MJ, Furlow PW, Lucas GS, Li X, Lappin TR, McMullin MF, Lee FS. A gain-of-function mutation in the HIF2A gene in familial erythrocytosis. N Engl J Med 358: 162-168, 2008.
46. Ries M, Basseau F, Tyndal B, Jones R, Deminière C, Catargi B, Combe C, Moonen CW, Grenier N. Renal diffusion and BOLD MRI in experimental diabetic nephropathy. Blood oxygen level-dependent. J Magn Reson Imaging 17: 104-113, 2003.
47. Rosenberger C, Khamaisi M, Abassi Z, Shilo V, Weksler-Zangen S, Goldfarb M, Shina A, Zibertrest F, Eckardt KU, Rosen S, Heyman SN. Adaptation to hypoxia in the diabetic rat kidney. Kidney Int 73: 34-42, 2008.
48. Salnikow K, Donald SP, Bruick RK, Zhitkovich A, Phang JM, Kasprzak KS. Depletion of intracellular ascorbate by the carcinogenic metals nickel and cobalt results in the induction of hypoxic stress. J Biol Chem 279: 4033-4044, 2004.
49. Schofield CJ, Ratcliffe PJ. Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol 5: 343-354, 2004.
50. Schroedl C, McClintock DS, Budinger GR, Chandel NS. Hypoxic but not anoxic stabilization of HIF-1alpha requires mitochondrial reactive oxygen species. Am J Physiol Lung Cell Mol Physiol 283: L922-L931, 2002.
51. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 3: 721-732, 2003.
52. Shih AY, Li P, Murphy TH. A small-molecule-inducible Nrf2-mediated antioxidant response provides effective prophylaxis against cerebral ischemia in vivo. J Neurosci 25: 10321-10335, 2005.
53. Siddiq A, Aminova LR, Troy CM, Suh K, Messer Z, Semenza GL, Ratan RR. Selective inhibition of hypoxia-inducible factor (HIF) prolylhydroxylase 1 mediates neuroprotection against normoxic oxidative death via HIF- and CREB-independent pathways. J Neurosci 29: 8828-8838, 2009.
54. Smith EL. Presence of cobalt in the anti-pernicious anaemia factor. Nature 162: 144, 1948.
55. Steinhoff A, Pientka FK, Möckel S, Kettelhake A, Hartmann E, Köhler M, Depping R. Cellular oxygen sensing: importins and exportins are mediators of intracellular localisation of prolyl-4-hydroxylases PHD1 and PHD2. Biochem Biophys Res Commun 387: 705-711, 2009.
56. Takeda K, Aguila HL, Parikh NS, Li X, Lamothe K, Duan LJ, Takeda H, Lee FS, Fong GH. Regulation of adult erythropoiesis by prolyl hydroxylase domain proteins. Blood 111: 3229-3235, 2008.
57. Takeda K, Ho VC, Takeda H, Duan LJ, Nagy A, Fong GH. Placental but not heart defects are associated with elevated hypoxia-inducible factor alpha levels in mice lacking prolyl hydroxylase domain protein 2. Mol Cell Biol 26: 8336-8346, 2006. (Pubitemid 44748568)
58. Tanaka T, Miyata T, Inagi R, Fujita T, Nangaku M. Hypoxia in renal disease with proteinuria and/or glomerular hypertension. Am J Pathol 165: 1979-1992, 2004.
59. Tong KI, Kobayashi A, Katsuoka F, Yamamoto M. Two-site substrate recognition model for the Keap1-Nrf2 system: a hinge and latch mechanism. Biol Chem 387: 1311-1320, 2006.
60. Tug S, Delos Reyes B, Fandrey J, Berchner-Pfannschmidt U. Nonhypoxic activation of the negative regulatory feedback loop of prolylhydroxylase oxygen sensors. Biochem Biophys Res Commun 384: 519-523, 2009.
61. Wakabayashi N, Itoh K, Wakabayashi J, Motohashi H, Noda S, Takahashi S, Imakado S, Kotsuji T, Otsuka F, Roop DR, Harada T, Engel JD, Yamamoto M. Keap1-null mutation leads to postnatal lethality due to constitutive Nrf2 activation. Nat Genet 35: 238-245, 2003.
62. Wang W, Fang H, Groom L, Cheng A, Zhang W, Liu J, Wang X, Li K, Han P, Zheng M, Yin J, Wang W, Mattson MP, Kao JP, Lakatta EG, Sheu SS, Ouyang K, Chen J, Dirksen RT, Cheng H. Superoxide flashes in single mitochondria. Cell 134: 279-290, 2008.
63. Watanabe D, Suzuma K, Matsui S, Kurimoto M, Kiryu J, Kita M, Suzuma I, Ohashi H, Ojima T, Murakami T, Kobayashi T, Masuda S, Nagao M, Yoshimura N, Takagi H. Erythropoietin as a retinal angiogenic factor in proliferative diabetic retinopathy. N Engl J Med 353: 782-792, 2005. (Pubitemid 41215487)
64. Wiener CM, Booth G, Semenza GL. In vivo expression of mRNAs encoding hypoxia-inducible factor 1. Biochem Biophys Res Commun 225: 485-488, 1996.
65. Yang ZZ, Zhang AY, Yi FX, Li PL, Zou AP. Redox regulation of HIF-1alpha levels and HO-1 expression in renal medullary interstitial cells. Am J Physiol Renal Physiol 284: F1207-F1215, 2003.
66. Yoh K, Hirayama A, Ishizaki K, Yamada A, Takeuchi M, Yamagishi S, Morito N, Nakano T, Ojima M, Shimohata H, Itoh K, Takahashi S, Yamamoto M. Hyperglycemia induces oxidative and nitrosative stress and increases renal functional impairment in Nrf2-deficient mice. Genes Cells 13: 1159-1170, 2008.
67. Yu AY, Frid MG, Shimoda LA, Wiener CM, Stenmark K, Semenza GL. Temporal, spatial, and oxygen-regulated expression of hypoxia-inducible factor-1 in the lung. Am J Physiol Lung Cell Mol Physiol 275: L818-L826, 1998.
68. Zhou F, Zhu X, Castellani RJ, Stimmelmayr R, Perry G, Smith MA, Drew KL. Hibernati on, a model of neuroprotection. Am J Pathol 158: 2145-2151, 2001.
69. Zhou F, Zhu X, Castellani RJ, Stimmelmayr R, Perry G, Smith MA, Drew KL. Hypoxia tolerance in mammalian heterotherms. J Exp Biol 207: 3155-3162, 2004.